ISSN 2308-4057 (Print),
ISSN 2310-9599 (Online)

137Cs and 40K activity concentrations in edible wild mushrooms from China regions during the 2014–2016 period

Abstract
Introduction. Contamination by radiocaesium of edible wild mushrooms after major nuclear accidents is a long-lasting process in some regions of the world. Following greater awareness of radioactive pollution in Asia, particularly after the Fukushima accident, this study investigated the radioactivity of 137Cs and 40K contamination in edible wild mushrooms in China.
Study objects and methods. The objects of the research were edible wild mushrooms collected during 2014 to 2016, from the Inner Mongolian and Yunnan regions of China. To obtain an insight into any environmental impacts to distant regions of mainland Asia, the mushrooms were analyzed for 137Cs activity. In parallel, the natural activity of 40K was also determined and used to estimate the content of total K. The topsoil underneath the mushrooms was also investigated from a few sites in Bayanhushu in Inner Mongolia in 2015.
Results and discussion. The results showed that in 4 to 6 mushrooming seasons after the accident, mushrooms from both regions were only slightly contaminated with 137Cs, which implied negligible consequences. The activity concentrations of 137Cs in dried caps and whole mushrooms in 63 of 70 lots from 26 locations were well below 20 Bq kg–1 dry weight. Two species (Lactarius hygrophoroides L. and Lactarius volemus L.), from Jiulongchi in Yuxi prefecture showed higher 137Cs activities, from 130 ± 5 to 210 ± 13 Bq kg–1 dw in the caps. 40K activities of mushrooms were around two- to three-fold higher. A composite sample of topsoil (0–10 cm layer) from the Bayanhushu site (altitude 920 m a.s.l.) in Inner Mongolia showed 137Cs activity concentration at a low level of 6.8 ± 0.7 Bq kg–1 dw, but it was relatively rich in potassium (40K of 595 ± 41 Bq kg–1 and total K of 17000 ± 1000 mg kg–1 dw).
Conclusion. Wild mushrooms from the Yunnan and Inner Mongolia lands only slightly affected with radioactivity from artificial 137Cs. Lack of 134Cs showed negligible impact from Fukushima fallout. Ionizing radiation dose from 137Cs in potential meals was a fraction of 40K radioactivity. The associated dietary exposure to ionizing irradiation from 137Cs and 40K contained in mushrooms from the regions studied was considered negligible and low, respectively. Mushroom species examined in this study are a potentially good source of dietary potassium.
Keywords
Asia , forest , fungi , pollution , soil , radioactivity , radiocaesium , wild food
INTRODUCTION

Radiocaesium (134/137Cs), if not mention the shortlived radioactive 131I (t0.5 = 8.02 days), is the main mass and a long-term source of the toxic radiation, polluting the Earth in the past from the nuclear weapon explosions and nuclear power plant accidents [1, 2].

Macromycetes (fungi) can accumulate various elements in their fruiting bodies, including radioactive isotopes (134Cs, 137Cs, 40K, 210Po, 210Pb, 238Pu, 239+240Pu,90Sr, 230Th, 232Th, 234U, 238U) emitting radiation of various toxicities [3–9]. Many wild fungi are effective accumulators of artificial radioactive cesium, which circulates in forest ecosystems for years in contaminated areas and can cause a potential health hazard from ingestion of the mushrooms [2, 10–14].

Radiocaesium (137Cs) is an artificial and long-lived (t0.5 = 30.1 years) nuclide, which appeared in mushrooms after global fallout from nuclear weapons detonations in the atmosphere. High levels of radioactivity reappeared following the collapse of the Chernobyl nuclear power plant in 1986, including massive levels of 134Cs and 137Cs emissions [15]. The consequent radioactive fallout caused a long-lasting and substantial contamination with 137Cs of forest ecosystems including mushrooms in regions surrounding the collapsed plant, especially in the Ukraine, Belarus and Russia, as well as elsewhere in Europe [16–23].

As in Chernobyl, a similar accident occurred in Japan in March 2011, where, following a major earthquake, a 15-meter tsunami disabled the power supply and cooling systems of three Fukushima Daiichi nuclear power plant reactors. All three cores largely melted in the first three days, caused radioactive contamination of the environment on a large scale, including high 137Cs pollution of fungi growing in the region [24–26].

The nuclear accidents caused long-term psychosocial consequences on exposed individuals. One of the consequences was that big game and domesticated ruminants that eat contaminated mushrooms could be also heavily loaded with 137Cs [27–29]. In humans, mushrooms can be also the most important exposure route to 137Cs when there is elevated consumption of wild species [30]. As mentioned, contamination by 137Cs after the Chernobyl accident as well as atomic weapon testing is a long-lasting process in some mushroom species even collected relatively away from this source [12–14].

The contribution of the 137Cs fallout from the Chernobyl accident to ecosystems in distant places like the Japanese islands was considered small compared to the previous global fallout [31]. The Chernobyl fallout had also some impacts on continental Asia. In China, soils (layer 0–10 cm) sampled from 56 sites in the Inner Mongolia province in 1982–1987 showed 137Cs mean activity concentration of 13.6 ± 6.6 Bq kg–1 dry weight (dw) (from 5.8 ± 4.4 to 23.4 ± 13.4 Bq kg–1 dw) [32]. Soil from Yunnan province was also contaminated, showing activity of 6.2 ± 5.4 Bq kg–1 dw (from 1.9 ± 0.3 to 31.6 ± 0.8 Bq kg–1 dw) in 1982–1987 [33].

The accident in the Fukushima nuclear power plant caused a high alert on a direct and indirect radioactive pollution consequences regarding to exposed staff and local residents. It affected public health and foods safety in Japan, as well as continental Asia from serious accidental discharge and included studies on the consequence to various types of environmental media including soils, vegetation and wild growing mushrooms [25, 34–46].

Edible mushrooms collected from the wild are common foodstuffs in Yunnan, a land diverse in climate, soil, forest types and landscape topography and with a high biodiversity of mushroom species [47, 48]. Certain species are conditionally edible or medicinal mushrooms, e.g. Caloboletus calopus (Pers.) Vizzini or Tricholoma sejunctum (Fr. ex Sow.) Quél. Inner Mongolia has an area of 1 183 000 km2 (457 000 sq mi) with a landscape made up largely of meadows with an abundance of saprobic mushrooms. This region is poor in ectomycorrhizal mushrooms, a result of the limited wooded areas, apart from the thickets along the Huang He River [49].

To get greater awareness of radioactive pollution in Asia, particularly after the Fukushima accident, this study investigated the radioactivity contamination with 137Cs and 40K of edible wild mushrooms from the Inner Mongolian and Yunnan provinces of China. The activity concentrations of 137Cs and 40K were studied for the first time in wild mushrooms (five species) from Inner Mongolia and also in more than 26 species, including taxa without previous data on 137Cs, from Yunnan, collected during 2014–2016.

STUDY OBJECTS AND METHODS

Mushroom and topsoil samples. Mushrooms were collected from the Inner Mongolia province (approximate distance from Fukushima Daiichi power plant site is 2500 km). They all represented saprobic species and included Agaricus arvensis Schaeff, Calocybe gambosa (Fr.) Donk, Calvatia gigantea (Batsch) Lloyd, Macrolepiota excoriata (Schaeff.) Wasser and Lepista personata (Fr.:Fr) Sing. The 26 species collected from Yunnan province (distance from Fukushima is in the range of 3500 to 4500 km) included Auricularia delicata (Fr.) Henn, Baorangia bicolor (Kuntze), Boletus bainiugan Dentinger, Boletus ferrugineus Schaeff., Hemileccinum impolitum (Fr.) Šutara, Boletus reticulatus Schaeff., Butyriboletus roseoflavus, Boletus tomentipes Earle, Caloboletus calopus (previous name Boletus calopus Fr.), Neoboletus brunneissimus (W.F. Chiu), Retiboletus griseus (Frost), Rubroboletus sinicus (W.F. Chiu), Sutorius magnificus (W.F. Chiu), Sutorius obscureumbrinus (Hongo), Laccaria vinaceoavellanea Hongo, Lactarius deliciosus (L.:Fr.) Gray, Lactarius hatsudake Tanaka, Lactarius hygrophoroides Berk. & M.A. Curtis, Lactarius volemus Fr., Lentinula edodes (Berk.) Pegler, Leccinum rugosiceps (Peck) Singer, Morchella esculenta Pers., Russula compacta Frost and Tricholoma sejunctum. The L. edodes samples were taken from cultivars from the Wuding in Chuxiong and Longyang in Baoshan from Yunnan, while solely composite samples were from Baise in Guangxi province and the Northeast of China. Soil samples were collected in parallel as two pooled samples of topsoil (0–10 cm layer) beneath the fruiting bodies of A. arvensis from grassy stands in the Bayanhushu site in Inner Mongolia. Details of the geographical locations of the sampling sites from which mushrooms and topsoil were collected are given in Fig. 1 and Table 1.

Figure 1 Localization of the sampling sites of mushrooms from the Inner Mongolia and Yunnan provinces in China

Table 1 137Cs and 40K activity concentration (± an instrumental counting error) and estimated K in mushrooms collected from the provinces of China

Preparation of materials. To examine the distribution of 137Cs and 40K and total K between the morphological parts, individual fruiting bodies were rinsed and separated into caps (with skin) and stipes, but some were examined as whole (Table 1). Before drying, the fungal materials were sliced into pieces using a ceramic knife and pooled to create composite samples representing each species, sampling location and time of collection. Mushroom parts were dried at 65°C to constant mass (Ultra FD1000 dehydrator, Ezidri, Australia), finely powdered in a porcelain mortar, passed through an 80-mesh sieve, and stored in screw sealed plastic (low density polyethylene) bags under dry conditions.

Two pooled samples of topsoil (0–10 cm layer; 150 g whole weight each) were cleaned from any visible pebbles, leaves and twigs, soil samples, air dried under clean condition, ground (porcelain mortar), sieved (2 mm mesh plastic sieve), and stored in sealed polyethylene bags.

Directly before analysis, the mushroom and soil materials were prophylactically deep frozen and lyophilized (Labconco Freeze Dry System, Kansas City, MO, USA) for three days to ensure full dehydration.

Instrumental analysis. The analytical methodology applied has been presented in detail before [43, 67, 68] but a summarized description is given below. In brief, activity concentrations of 137Cs, 134Cs and 40K were measured using a γ-spectrometer with a coaxial HPGe detector with a relative efficiency of 18% and a resolution of 1.9 keV at 1.332 MeV of 60Co (with associated electronics) (Detector GC 1819 7500 SL, Canberra Packard, Poland, Warsaw). The measurements of the fungal materials in this study were preceded by background measurement (time 80 000 s) and counting time was similar (> 22 h).

The instrument was calibrated using a multiisotope standard by validated methodology. The reference solution (Standard solution of gamma emitting isotopes, code BW/Z-63/48/16), obtained from the IBJŚwierk near Otwock in Poland, was used to prepare reference samples for equipment calibration. The radionuclides used in the reference solution during equipment calibration were 241Am (1.2%), 109Cd (2.1%), 57Co (0.80%), 51Cr (1.55%), 113Sn (2.0%), 85Sr (1.2%), 137Cs (1.5%), 54Mn (1.55%), 65Zn (1.2%) and 60Co (0.8%). The same geometry of cylindrical dishes with a 40-mm diameter was used for the analysis of the fungal material extracts as well as for the reference samples during equipment calibration organized by IAEARML-2018-01. Detailed results of the intercalibration are available in the publication [50].

Minimum detectable activity was determined by the Currie method. This method is based on two basic parameters: (a) critical level, which is defined as a level below which the detection signal cannot be reliably recognized and (b) detection limit specifying the smallest signal that can be quantitatively reliable. The measurement results obtained were recalculated for dehydrated materials and decay corrected back to the time of collection. Total potassium content was calculated from the original 40K activity concentration data (using mean value of 29.32 Bq g–1) in natural K, which is in the range from 27.33 to 31.31 Bq g–1 of K (percentage abundance of 40K atoms in natural K is 0.0117%) [51].

RESULTS AND DISCUSSION

137Cs and 134Cs in mushrooms and soil. All species collected from Inner Mongolia in this study were saprobic. 134Cs activity was not detected in any of the study samples. It was possibly due to the negligible impact from the Fukushima’s fallout in 2011 as wells as a relatively short half-life of this isotope (t0.5 = 2.1 years) and small impacts from the Chernobyl’s fallout in 1986 and preceding, the nuclear weapons detonations in the atmosphere.

The values of the activity concentration of 137Cs in caps and stipes of the fruiting bodies of Agaricus arvensis, Calocybe gambosa, Lepista personata and Macrolepiota excoriata and in the whole fruiting bodies of C. gigantea were in the range from < 4.1 to 19 ± 4 Bq kg–1 dw (Table 1). There is no prior data for these species from regions of Asia other than Inner Mongolia [44, 53, 54]. The low levels of 137Cs contamination in the studied mushrooms from the Inner Mongolian region reflects low activities of this nuclide in local soils as well as a lower potential of these species to bio-accumulate this nuclide.

In this study, a composite sample of the upper (0–10 cm) layer of soil collected in parallel with A. arvensis from the Bayanhushu site (altitude 920 m a.s.l.) showed 137Cs activity concentration of 6.8 ± 0.7 Bq kg–1 dw. This result obtained for the sample from 2015 is around 2 to 4-fold lower than earlier results cited for topsoils collected in Inner Mongolia in 1982– 1987, and is close to the activity values reported in 1–5 cm layer of forest topsoils sampled from the Changning and Mengman sites in Yunnan in 2016 (4.9 ± 0.6 and 7.5 ± 0.7 Bq kg–1 dw) [53].

Because of colder weather in the mountains, soil and the mushrooms can be specifically affected with radiocaesium, which is scavenged from the contaminated plumes by wet precipitation [53–55]. Forest topsoil collected at 3000 m above sea level from the Minya Konka (Gongga Shan) mountain in Sichuan province of China in 2012 showed 137Cs at level from 41 ± 1 to 79 ± 2 Bq kg–1 dw. This result is well in excess of what has been noted in topsoil from Inner Mongolia in this study or other studies of soils from China [32, 33, 53].

As given in Table 1, the determined activity concentrations of 137Cs in fruiting bodies of the saprobic and perhaps a little parasitic species of Auricularia delicate, the caps and stipes of fruiting bodies of the saprobic decomposer Lentinula edodes, the saprobic Morchella esculenta as well as over 20 species of mycorrhizal mushrooms collected in Yunnan were low and roughly in the range of values noted in mushrooms from Inner Mongolia.

The only exception was individuals of Lactarius hygrophoroides collected from the region of Jiulongchi in Yuxi prefecture in central Yunnan in the summer of 2016. They showed activity concentrations of 137Cs from 130 ± 5 to 210 ± 13 Bq kg dw–1 in caps and from 60 ± 5 to 67 ± 7 Bq kg dw–1 in stipes (Table 1). These relatively high levels of 137Cs activity in L. hygrophoroides from the Jiulongchi site were in the range of activities determined previously in several species of ectomycorrhizal mushrooms collected at 2900– 3600 m above sea level from the Minya Konka summit in 2012 [53].

Many other species of mushrooms collected from the prefecture of Yuxi and across other regions from Yunnan and elsewhere in China (Zhangzhou in the Fujian province) in 2010‒2018 were substantially less contaminated than L. hygrophoroides from the Jiulongchi site or even mushrooms from the subalpine regions on the eastern slope of the Minya Konka summit [12, 16, 42, 44, 47, 52, 53, 56]. The exception was Turbinellus floccosus (Schwein.) Earle ex Giachini & Castellano [previous name Gomphus floccosus (Schw.) Singer] collected from the region of Mangshi (98°24’ E, 24°22’ N) in the western part of Yunnan during August 2012 to July 2013, which showed a 137Cs activity concentration of 212 (148–339) Bq kg–1 dw in the whole fruiting bodies [44, 57].

Elevated activity concentrations of 137Cs in L. hygrophoroides from the Jiulongchi site in this study can possibly be explained by weather conditions (episodic rain) scavenging nuclides from the radioactive plume after the Fukushima (Japan) nuclear power plant accident in early 2011.

The radioactive incident took place in Tongchuan, Shaanxi Province, south of the central region of Inner Mongolia (approximate distance from the sampling sites mushrooms there is 1200 km). Some 137Cs from a measuring instrument (lead ball – a major component of a nuclear scale) when dismantling a cement factory has gone missing. In a later investigation, radioactivity from 137Cs was found at a steel refinery in Shaanxi’s Fuping county. Possibly, a lead ball with scrap metal was melted down into the steel [58]. Information on possible, if any, ground pollution in the region from this accident is not available.

A recent (2021) study showed that the activity concentration of 137Cs in 66 out of 68 of wild mushrooms (17 species) collected from the northeast regions of China in 2017‒2020 ranged from < 0.6 to 26 Bq kg–1 dw (data rounded), and only in single Lactarius deliciosus and Lepista nuda (Bull.) Cooke specimens collected in 2020, was 46 ± 3 Bq kg–1 dw and 130 ± 9 Bq kg–1 dw, respectively [59].

The maximum activity concentration of 137Cs noted in L. nuda in the above mentioned study was close to values determined in Lactarius hygrophroides and Lactarius volemus from Jiulongchi, Yuxi (Yunnan) (Table 1), while the results are not very comparable due to only two single specimens examined by Wang et al. [59].

The radiocaesium contamination of land, the oceans and biota, including edible wild growing mushrooms has thus far, occurred in three main waves. The first one arose from the nuclear weapons detonations in the atmosphere in the period from 1945 to 1980 and resulted in wide-spread aerial diffusion of radiocaesium and other nuclides including 14C, 137Cs, 90Sr, 239–240Pu, 241Am and 3H [60]. With time, the resulting depositions of longer lasting 137Cs affected every region of the world [1, 60].

Data on radiocaesium in mushrooms for the period before 1986 is scarce [10–13, 42, 61]. Fifteen years before the Chernobyl accident, a solely fruiting body of Tricholoma terreum collected from the Czech Republic in 1971 showed 137Cs at a level of 40 Bq kg–1 dw [61]. Additional historical data on 137Cs in mushrooms was recorded in 1984, in Poland for the Poison Pax (Paxillus involutus), which showed 137Cs at a level of 2700 Bq kg–1 dw, with lower levels noted for the King Bolete (Boletus edulis) (95 and 104 Bq kg–1 dw) and Slippery Jack, Suillus luteus (125 and 150 Bq kg–1 dw) collected in 1984 and 1985, respectively [10].

Data on the radiocaesium concentration activities accumulated in wild mushrooms growing in Asia from the period before the Chernobyl accident are absent in the available literature. Effectively, there is also nothing published on radiocaesium in wild mushrooms from mainland Asia in the period between the Chernobyl and Fukushima incidents.

The Chernobyl emission of radioactivity caused an extreme and long-lasting radiocaesium pollution of wild growing mushrooms in the regions of Europe, and particularly in the neighbor areas collapsed nuclear power plant [12, 16, 17, 62–65]. Japanese researchers have published a large volume of data on artificial radioactivity accumulated in wild mushrooms growing in the country, both from the post-Chernobyl and post-Fukushima emissions, which have recently been evaluated by Komatsu et al. and Prand-Stritzko and Steinhauser [25, 66]. The activity in these wild mushrooms collected in the period up to March 2011 was largely from accumulated radiocaesium (137Cs) due to the global fallout from nuclear weapons detonations, with a small proportion being attributed to the Chernobyl emissions [54]. The more recent emissions from the Fukushima incident changed the pattern of radionuclide contamination of wild mushrooms in Japan. However, as shown in this study (Table 1) and in a few other reports, the emissions could have only a small impact on mainland Asia or elsewhere [44, 53, 68–69].

40K and K in mushrooms and soil. The topsoil from the Bayanhushu site showed 40K activity concentration of 595 ± 41 Bq kg–1 dw and total K content of 17 000 ± 1000 mg kg–1 dw, which were higher than previously determined in topsoils sampled from several forested areas in Yunnan (150 ± 14 to 340 ± 19 Bq kg–1 dw) [53].

In the study by Zhang et al., the means of 40K activity concentrations in topsoils (0–10 cm) in Inner Mongolia and Yunnan in 1982–1987 were 755 (866–1066 Bq kg–1 dw) and 487 Bq kg–1 dw (149–1010 Bq kg–1 dw), respectively [70]. In another national survey performed during 1983–1990, the area-weighted mean and the point-weighted mean of 40K were 655.6 and 624.6 Bq kg–1 dw, respectively, for soils in Inner Mongolia, while the two values for soils from Yunnan were 532.0 and 518.6 Bq kg–1 dw, respectively [71].

The activity concentrations of 40K in mushrooms from Inner Mongolia were in the range of 875 ± 140 to 1600 ± 320 Bq kg–1 dw in caps and from 1100 ± 180 to 1400 ± 620 Bq kg–1 dw in stipes (Table 1). In the case of mushrooms from Yunnan, A. delicate (ear-like jelly fungus), which grows on wood, they had a lower activity concentration of 40K (540 ± 61 Bq kg–1 dw) than L. edodes (Table 1), which also grows on wood. The L. edodes showed activities in the range of 790 ± 110 to 1200 ± 140 Bq kg–1 dw in the caps, which are culinary valued, and from 640 ± 88 to 1100 ± 240 Bq kg–1 dw in the stipes, which are largely discarded. This species collected from Yunnan and examined by other authors, demonstrated the mean value of 40K activity concentration to be 629 Bq kg–1 dw (from 396 to 1010 Bq kg–1 dw; n = 11) [44]. 40K values in the caps of terrestrial mushrooms from Yunnan were from 580 ± 110 Bq kg–1 dw in L. deliciosus to 4000 ± 680 Bq kg–1 dw in Boletus tomentipes, while stipes showed activities from 380 ± 78 Bq kg–1 dw in L. deliciosus to 1900 ± 340 Bq kg–1 dw in Tricholoma sejunctum.

Potassium (total K) is the major metallic element in mushrooms and occurs in dried fungal materials in quantities of up to several percent, while the natural nuclide 40K forms only a small proportion (makes up 0.012%) of the total. Hence, mushrooms collected from areas that are only mildly affected by 137Cs depositions or mushrooms without a high species-specific ability to bioconcentrate this nuclide, e.g. like some species from the genus Cortinarius, contained natural 40K in high excess relative to 137Cs (Table 1) [12].

The amounts of K in the caps, stipes, or whole fruiting bodies of the species in this study were in the range 16 000 to 120 000 mg kg–1 dw (1.6 to 12 g kg–1 dw). Potassium is indispensable for mushrooms, for the uptake and osmotic regulation of water in the cytoplasm of cells and is a co-factor in certain enzymes [72]. However, the same species, i.e. A. arvensis, Boletus bainiugan, Retiboletus griseus, Rubroboletus sinicus, Caloboletus calopus, L. hygrophoroides, L. edodes and T. sejunctum collected from different sites could differ around twofold in the content of K (Table 1).

The daily adequate intake of K for adults is 2300 mg for females and 3400 mg for males [73]. Thus, the mushroom species examined in this study and assuming absorption rate at around 90% could be considered as potentially good sources of dietary potassium, especially when stir-fried with oil, which is a common culinary technique in SW China [67].

Potential risk from ionizing radiation doses. In this study, a total of 70 lots of several species of edible mushrooms collected from 26 locations in Yunnan were examined and in 63 lots, the contamination with 137Cs of the caps or the whole mushrooms was well below 20 Bq kg–1 dw (Table 1). There were three of 70 lots that were more contaminated with 137Cs than the others. Those lots were the gilled mushroom B. tomentipes (of 69 ± 4 Bq kg–1 dw), caps of the lamellar mushroom L. hygrophoroides (130 ± 5 Bq kg–1 dw), and caps of lamellar L. volemus (210 ± 13 Bq kg–1 dw) (Table 1). Assuming that the moisture content in fruiting bodies is 90%, the estimated 137Cs activities in these three species were 6.9, 13, and 21 Bq kg–1 on a wet weight basis. Therefore, these amounts were much lower than the maximum permitted levels for import of mushrooms from third countries [specific 13 countries affected by the Chernobyl’s radioactive fallout for which the regulation applies] to the European Union (600 Bq kg–1)[74].

In Yunnan, the main way to cook mushrooms is stirfrying in vegetable oil in a wok pan [75]. It is interesting that stir-fried mushroom meals showed about 2 to 5-fold higher activity concentrations of 137Cs than the raw mushrooms on a whole weight (wet) basis [67, 68].

Therefore, a 100-g portion of stir-fried L. volemus caps from the most contaminated lot in this study could include from 4.2 to 10.5 Bq of 137Cs (equivalent to ionizing radiation dose from 56×10–3 to 140×10–3 µSv per capita or 0.49×10–3 to 2.35×10–3 µSv per kg body mass; 60 kg body mass). These estimates are low, taking into account the risk associated with the doses of ionizing radiation received by consumers in Yunnan, even if stirfried mushrooms are consumed daily for longer periods during the mushrooming season.

In comparison, the natural 40K nuclide contained in mushrooms (Table 1) introduces much higher doses of ionizing radiation than 137Cs for locals in Inner Mongolia and Yunnan provinces but is not considered as a hazardous nuclide for consumers due to homeostasis of K in human body.

CONCLUSION

The activity concentrations of 137Cs in lamellar mushrooms from the Inner Mongolia province of China and the local soil were low. 137Cs contamination of the lamellar and gilled mushrooms from Yunnan province in China was also low, i.e. well below one tenth of statutory limits, and mushroom meals there can be considered as a negligible source of 137Cs for their consumers.

In view of the results from this study, the accident in the Fukushima nuclear power plant had little or negligible effect on radioactive contamination of edible and medicinal fungi in the regions of China. Natural nuclide 40K contained in mushrooms is not considered as hazardous for mushroom meal consumers. Wild mushrooms can be considered as a good source of dietary potassium for consumers.

CONFLICTS OF INTEREST
The authors declare no conflict of interests regarding the publication of this article.
REFERENCES
  1. Aoyama M, Hirose K, Igarashi Y. Re-construction and updating our understanding on the global weapons tests 137Cs fallout. Journal of Environmental Monitoring. 2006;8(4):431–438. https://doi.org/10.1039/b512601k.
  2. Dementyew D, Bolsunovsky A. A long-term study of radionuclide concentrations in mushrooms in the 30-km zone around the Mining-and-Chemical Combine (Russia). Isotopes in Environmental and Health Studies. 2020;56(1):83–92. https://doi.org/10.1080/10256016.2020.1718124.
  3. Daillant O, Boilley D, Josset, M, Hettwig B, Fischer HW. Evolution of radiocaesium contamination in mushrooms and influence of treatment after collection. Journal of Radioanalytical and Nuclear Chemistry. 2013;297(3):437–441. https://doi.org/10.1007/s10967-012-2411-9.
  4. Lehto J, Vaaramaa K, Leskinen A. 137Cs, 239,240Pu and 241Am in boreal forest soil and their transfer into wild mushrooms and berries. Journal of Environmental Radioactivity. 2013;116:124–132. https://doi.org/10.1016/j.jenvrad.2012.08.012.
  5. Saniewski M, Zalewska T, Krasińska G, Szylke N, Wang Y, Falandysz J. 90Sr in King Bolete Boletus edulis and certain other mushrooms consumed in Europe and China. Science of the Total Environment. 2016;543:287–294. https://doi.org/10.1016/j.scitotenv.2015.11.042.
  6. Szymańska K, Strumińska-Parulska D, Falandysz J. Isotopes of 210Po and 210Pb in Hazel bolete (Leccinellum pseudoscabrum) – bioconcentration, distribution and related dose assessment. Environmental Science and Pollution Research. 2019;26(18):18904–18912. https://doi.org/10.1007/s11356-019-05376-8.
  7. Falandysz J, Saba M, Strumińska-Parulska D. 137Caesium, 40K and total K in Boletus edulis at different maturity stages: Effect of braising and estimated radiation dose intake. Chemosphere. 2021;268. https://doi.org/10.1016/j.chemosphere.2020.129336.
  8. Strumińska-Parulska D, Falandysz J. A review of the occurrence of alpha-emitting radionuclides in wild mushrooms. International Journal of Environmental Research and Public Health. 2020;17(21). https://doi.org/10.3390/ijerph17218220.
  9. Strumińska-Parulska D, Falandysz J, Moniakowska A. Beta-emitting radionuclides in wild mushrooms and potential radiotoxicity for their consumers. Trends in Food Science and Technology. 2021;114:672–683. https://doi.org/10.1016/j.tifs.2021.06.015.
  10. Bem H, Lasota W, Kuśmierek E, Witusik M. Accumulation of 137Cs by mushrooms from Rogozno area of Poland over the period 1984–1988. Journal of Radioanalytical and Nuclear Chemistry Letters. 1990;145(1):39–46. https://doi.org/10.1007/BF02328766.
  11. Johnson W, Nayfield CL. Elevated levels of cesium-137 in common mushrooms (Agaricaceae) with possible relationship to high levels of cesium-137 in Whitetail deer, 1968–1969. Radiological Health Data and Reports. 1970;11(19):527–531.
  12. Falandysz J, Zalewska T, Fernandes AR. 137Cs and 40K in Cortinarius caperatus mushrooms (1996–2016) in Poland – Bioconcentration and estimated intake: 137Cs in Cortinarius spp. from the Northern Hemisphere from 1974 to 2016. Environmental Pollution. 2019;255. https://doi.org/10.1016/j.envpol.2019.113208.
  13. Falandysz J, Zalewska T, Saniewski M, Fernandes AR. An evaluation of the occurrence and trends in 137Cs and 40K radioactivity in King Bolete Boletus edulis mushrooms in Poland during 1995–2019. Environmental Science and Pollution Research. 2021;28(25):32405–32415. https://doi.org/10.1007/s11356-021-12433-8.
  14. Falandysz J, Saniewski M, Fernandes AR, Meloni D, Cocchi L, Strumińska-Parulska D, et al. Radiocaesium in Tricholoma spp. from the Northern Hemisphere in 1971–2016. Science of the Total Environment. 2022;802. https://doi.org/10.1016/j.scitotenv.2021.149829.
  15. Steinhauser G, Brandl A, Johnson TE. Comparison of the Chernobyl and Fukushima nuclear accidents: A review of the environmental impacts. Science of the Total Environment. 2014;470–471:800–817. https://doi.org/10.1016/j.scitotenv.2013.10.029.
  16. Falandysz J, Zalewska T, Krasińska G, Apanel A, Wang Y, Pankavec S. Evaluation of the radioactive contamination in Fungi genus Boletus in the region of Europe and Yunnan Province in China. Applied Microbiology and Biotechnology. 2015;99(19):8217–8224. https://doi.org/10.1007/s00253-015-6668-0.
  17. Grodzinskaya AA, Syrchin SA, Kuchma ND, Wasser SP. Macromycetes accumulative activity in radionuclide contamination conditions of the Ukraine territory. In: Zhdanova NN, Zakharchenko VA, Vasilevskaya AI, Shkolʹnyy AT, Kuchma ND, Artyshkova LV, et al., editors. Mycobiota of Ukrainian Polesie: Consequences of the Chernobyl disaster. Kiev: Naukova dumka; 2013. pp. 217–260.
  18. Betti L, Palego L, Lucacchini,A, Giannaccini G. 137Caesium in samples of wild-grown Boletus edulis Bull. from Lucca province (Tuscany, Italy) and other Italian and European geographical areas. Food Additives and Contaminants – Part A Chemistry, Analysis, Control, Exposure and Risk Assessment. 2017;34(1):49–55. https://doi.org/10.1080/19440049.2016.1256502.
  19. Čadová M, Havránková R, Havránek J, Zölzer F. Radioactivity in mushrooms from selected locations in the Bohemian Forest, Czech Republic. Radiation and Environmental Biophysics. 2017;56(2):167–175. https://doi.org/10.1007/s00411-017-0684-7.
  20. Cocchi L, Kluza K, Zalewska T, Apanel A, Falandysz J. Radioactive caesium (134Cs and 137Cs) in mushrooms of the genus Boletus from the Reggio Emilia in Italy and Pomerania in Poland. Isotopes in Environmental and Health Studies. 2017;53(6):620–627. https://doi.org/10.1080/10256016.2017.1337761.
  21. Türkekul I, Yeşilkanat CM, Cirişc A, Kölemend U, Çevikc U. Interpolated mapping and investigation of environmental radioactivity levels in soils and mushrooms in the Middle Black Sea Region of Turkey. Isotopes in Environmental and Health Studies. 2018;54(3):262–273. https://doi.org/10.1080/10256016.2017.1402768.
  22. Zalewska T, Cocchi L, Falandysz J. Radiocaesium in Cortinarius spp. mushrooms in the regions of the Reggio Emilia in Italy and Pomerania in Poland. Environmental Science and Pollution Research. 2016;23(22):23169–23174. https://doi.org/10.1007/s11356-016-7541-0.
  23. Tucaković I, Barišić D, Grahek Ž, Kasap A, Širić I. 137Cs in mushrooms from Croatia sampled 15–30 years after Chernobyl. Journal of Environmental Radioactivity. 2018;181:147–151. https://doi.org/10.1016/j.jenvrad.2017.11.004.
  24. Cui L, Orita M, Taira Y, Takamura N. Radiocesium concentrations in mushrooms collected in Kawauchi Village five to eight years after the Fukushima Daiichi Nuclear Power Plant accident. PLoS ONE. 2020;15(9). https://doi.org/10.1371/journal.pone.0239296.
  25. Komatsu M, Nishina K, Hashimoto S. Extensive analysis of radiocesium concentrations in wild mushrooms in eastern Japan affected by the Fukushima nuclear accident: Use of open accessible monitoring data. Environmental Pollution. 2019;255. https://doi.org/10.1016/j.envpol.2019.113236.
  26. Orita M, Nakashima K, Taira Y, Fukuda T, Fukushima Y, Kudo T, et al. Radiocesium concentrations in wild mushrooms after the accident at the Fukushima Daiichi Nuclear Power Station: Follow-up study in Kawauchi village. Scientific Reports. 2017;7(1). https://doi.org/10.1038/s41598-017-05963-0.
  27. Smith FB. The deposition of Chernobyl caesium-137 in heavy rain and its persistent uptake by grazing sheep. Agricultural and Forest Meteorology. 1994;47(2–4):163–177. https://doi.org/10.1016/0168-1923(89)90094-4.
  28. Steiner M, Fielitz U. Deer truffles – the dominant source of radiocaesium contamination of wild boar. Radioprotection. 2009;44(5):585–588. https://doi.org/10.1051/radiopro/20095108.
  29. Steinhauser G, Saey PRJ. 137Cs in the meat of wild boars: a comparison of the impacts of Chernobyl and Fukushima. Journal of Radioanalytical and Nuclear Chemistry. 2016;307(3):1801–1806. https://doi.org/10.1007/s10967-015-4417-6.
  30. Stijve T. Extraction of radiocesium from contaminated mushrooms. Observations Mycologiques (Bulletin de l’Observatoire Mycologique). 1994;6:2–9.
  31. Igarashi Y, Otsuji-Hatori M, Hirose K. Recent deposition of 90Sr and 137Cs observed in Tsukuba. Journal of Environmental Radioactivity. 1996;31(2):157–169. https://doi.org/10.1016/0265-931X(96)88491-8.
  32. Zhao Z, Ma L. Levels of radionuclides in soils from Inner Mongolia. Chinese Journal of Radiological Medicine and Protection. 1988;8(2):31–35. (In Chinese).
  33. An G, Liu P, Xiong J, Hu P. Content and distribution of radionuclides in soils from Yunnan province. Chinese Journal of Radiological Medicine and Protection. 1988;8(2):101–104. (In Chinese).
  34. Hirose K. Fukushima Daiichi Nuclear Plant accident: Atmospheric and oceanic impacts over the five years. Journal of Environmental Radioactivity. 2016;157:113–130. https://doi.org/10.1016/j.jenvrad.2016.01.011.
  35. Liu LB, Wu S, Cao JJ, Xie F, Shi QL, Zhang CY, et al. Monitoring of atmospheric radionuclides from the Fukushima nuclear accident and assessing their impact on Xi’an, China. Chinese Science Bulletin. 2013;58(13):1585–1591. https://doi.org/10.1007/s11434-012-5521-4.
  36. Hsu S-C, Huh C-A, Chan C-Y, Lin S-H, Lin F-J, Liu SC. Hemispheric dispersion of radioactive plume laced with fission nuclides from the Fukushima nuclear event. Geophysical Research Letters. 2012;39(1). https://doi.org/10.1029/2011GL049986.
  37. Melgunov MS, Pokhilenko NP, Strakhovenko VD, Sukhorukov FV, Chuguevskii AV. Fallout traces of the Fukushima NPP accident in southern West Siberia (Novosibirsk, Russia). Environmental Science and Pollution Research. 2012;19(4):1323–1325. https://doi.org/10.1007/s11356-011-0659-1.
  38. Qiao FL, Wang GS, Zhao W, Zhao JC, Dai DJ, Song YJ, et al. Predicting the spread of nuclear radiation from the damaged Fukushima Nuclear Power Plant. Chinese Scientific Bulletin. 2011;56(18):1890–1896. https://doi.org/10.1007/s11434-011-4513-0.
  39. Sheng L, Zhou B, Sun M, Lu K, Tong H, Hu J. Atmospheric radioactive fallout in China due to the Fukushima nuclear plant accident. Meteorological Monthly. 2013;39:1490–1499. (In Chinese).
  40. Shuai Z, Zhao Q, Pang R, Ouyang J, Liu P, Wang Q. Impact of Japan’s Fukushima nuclear accident on the radiation environment of Sichuan Province. Sichuan Environment. 2016;35:92–97. (In Chinese).
  41. Wan E, Zheng X, Wang S, Wan G, Wang C. Atmospheric pollutants transport tracks revealed from 131I, 137Cs, and 134Cs leaked from Fukushima accident and 7Be and 210Pb observed at Guiyang of China. Chinese Journal of Geochemistry. 2014;33(3):248–255. https://doi.org/10.1007/s11631-014-0684-0.
  42. Falandysz J, Zalewska T, Apanel A, Drewnowska M, Kluza K. Evaluation of the activity concentrations of 137Cs and 40K in some Chanterelle mushrooms from Poland and China. Environmental Science and Pollution Research. 2016;23(19):20039–20048. https://doi.org/10.1007/s11356-016-7205-0.
  43. Falandysz J, Wang Y, Saniewski M. 137Cs and 40K activities and total K distribution in the sclerotia of the Wolfiporia cocos fungus from China. Journal of Environmental Radioactivity. 2021;231. https://doi.org/10.1016/j.jenvrad.2021.106549.
  44. Tuo F, Zhang J, Li W, Yao S, Zhou Q, Li Z. Radionuclides in mushrooms and soil-to-mushroom transfer factors in certain areas of China. Journal of Environmental Radioactivity. 2017;180:59–64. https://doi.org/10.1016/j.jenvrad.2017.09.023.
  45. Wang J-J, Wang C-J, Lai S-Y, Lin Y-M. Radioactivity concentrations of 137Cs and 40K in Basidiomycetes collected in Taiwan. Applied Radiation and Isotopes. 1998;49(1–2):29–34. https://doi.org/10.1016/S0969-8043(97)00249-2.
  46. Wang Q, Pang R, Zhao Q, Ouyang J. Survey on the radioactivity level of γ nuclides in partial ecosystem and food chain in Sichuan province after Japan's Fukushima nuclear accident. Sichuan Environment. 2014;33:7–13. (In Chinese).
  47. Falandysz J, Zhang J, Zalewska T. Radioactive artificial 137Cs and natural 40K activity in 21 edible mushrooms of the genus Boletus species from SW China. Environmental Science and Pollution Research. 2017;24(9):8189–8199. https://doi.org/10.1007/s11356-017-8494-7.
  48. Wu F, Zhou L-W, Yang Z-L, Bau T, Li T-H, Dai Y0C. Resource diversity of Chinese macrofungi: edible, medicinal and poisonous species. Fungal Diversity. 2020;98(1). https://doi.org/10.1007/s13225-019-00432-7.
  49. Liu X, Guo J, Wang S, Li Y, Na R. Identification of several edible mushrooms in Inner Mongolia by rDNA-ITS. Edible and Medicinal Mushrooms. 2015;23:301–306. (In Chinese).
  50. Saniewski M, Wietrzyk-Pełka P, Zalewska T, Osyczka P, Węgrzyn MH. Impact of distance from the glacier on the content of 137Cs and 90Sr in the lichen Cetrariella delisei. Chemosphere. 2020;259. https://doi.org/10.1016/j.chemosphere.2020.127433.
  51. Samat SB, Green S, Beddoe AH. The 40K activity of one gram of potassium. Physics in Medicine and Biology. 1997;42(2):407–413. https://doi.org/10.1088/0031-9155/42/2/012.
  52. Wang Y, Zalewska T, Apanel A, Zhang J, Maćkiewicz Z, Wiejak A, et al. Artificial 137Cs, 134Cs and natural 40K in sclerotia of Wolfiporia extensa fungus collected across of the Yunnan land in China. Journal of Environmental Science and Health – Part B Pesticides, Food Contaminants, and Agricultural Wastes. 2015;50(9):654–658.
  53. Falandysz J, Saniewski M, Zhang J, Zalewska T, Liu H-G, Kluza K. Artificial 137Cs and natural 40K in mushrooms from the subalpine region of the Minya Konka summit and Yunnan Province in China. Environmental Science and Pollution Research. 2018;25(1):615–627. https://doi.org/10.1007/s11356-017-0454-8.
  54. Bakken LR, Olsen RA. Accumulation of radiocaesium in fungi. Canadian Journal of Microbiology. 1990;36(10):704–710. https://doi.org/10.1139/m90-119.
  55. Movsisyan N, Demirtchyan G, Pyuskyulyan K, Belyaeva O. Identification of radionuclides’ altitudinal distribution in soil and mosses in highlands of Armenia. Journal of Environmental Radioactivity. 2021;31. https://doi.org/10.1016/j.jenvrad.2021.106550.
  56. Falandysz J, Zhang J, Zalewska T, Apanel A, Wang Y, Wiejak A. Distribution and possible dietary intake of radioactive 137Cs, 40K and 226Ra with the pantropical mushroom Macrocybe gigantea in SW China. Journal of Environmental Science and Health – Part A Toxic/Hazardous Substances and Environmental Engineering. 2015;50(9):941–945.
  57. Tuo F, Xu C, Zhang J, Li W, Zhou Q, Zhang Q, et al. Measurement of activity concentrations for 137Cs and 40K in edible wild mushrooms collected from Mangshi Yunnan province and evaluation of dose to adult. Chinese Journal of Radiological Medicine and Protection. 2014;34:621–625. (In Chinese).
  58. Caesium-137 [Internet]. [cited 2021 Dec 14]. Available from: https://en.wikipedia.org/wiki/Caesium-137#2009_Tongchuan,_Shaanxi,_China.
  59. Wang S, Yang B, Zhou Q, Li Z, Li W, Zhang J, et al. Radionuclide content and risk analysis of edible mushrooms in northeast China. Radiation Medicine and Protection. 2021;2(4):165–170. https://doi.org/10.1016/j.radmp.2021.10.001.
  60. Prăvălie R. Nuclear weapons tests and environmental consequences: A global perspective. Ambio. 2014;43(6):729–744. https://doi.org/10.1007/s13280-014-0491-1.
  61. Klán J, Řanda Z, Benada J, Horyna J. Investigation of non-radioactive Rb, Cs, and radiocaesium in higher fungi. Czech Mycology. 1988;42:158–169. (In Czech).
  62. Kojta AK, Zhang J, Wang Y, Li T, Saba M, Falandysz J. Mercury contamination of fungi genus Xerocomus in the Yunnan Province in China and the region of Europe. Journal of Environmental Science and Health – Part A Toxic/Hazardous Substances and Environmental Engineering. 2015;50(13):1342–1350. https://doi.org/10.1080/10934529.2015.1059108.
  63. Grodzinskaya AA, Berreck M, Wasser SP, Haselwandter K. Radiocesium in fungi: accumulation pattern in the Kiev district of Ukraine including the Chernobyl zone. Sydowia. 1995;10:88–96.
  64. Strandberg M. Long-term trends in the uptake of radiocesium in Rozites caperatus. Science of the Total Environment. 2004;327(1–3):315–321. https://doi.org/10.1016/j.scitotenv.2004.01.022.
  65. Orita M, Kimura Y, Taira Y, Fukuda T, Takahashi J, Gutevych O, et al. Activities concentration of radiocesium in wild mushroom collected in Ukraine 30 years after the Chernobyl power plant accident. PeerJ. 2018;2018(1). https://doi.org/10.7717/peerj.4222.
  66. Prand-Stritzko B, Steinhauser G. Characteristics of radiocesium contaminations in mushrooms after the Fukushima nuclear accident: evaluation of the food monitoring data from March 2011 to March 2016. Environmental Science and Pollution Research. 2018;25(3):2409–2416. https://doi.org/10.1007/s11356-017-0538-5.
  67. Falandysz J, Zhang J, Saniewski M. 137Cs, 40K, and K in raw and stir-fried mushrooms from the Boletaceae family from the Midu region in Yunnan, Southwest China. Environmental Science and Pollution Research. 2020;27(26):32509–32517. https://doi.org/10.1007/s11356-020-09393-w.
  68. Falandysz J, Zhang J, Saniewski M, Wang Y. Artificial (137Cs) and natural (40K) radioactivity and total potassium in medicinal fungi from Yunnan in China. Isotopes in Environmental and Health Studies. 2020;56(3):324–333. https://doi.org/10.1080/10256016.2020.1741574.
  69. Muramatsu Y, Yoshida S. Mushroom and radiocesium. Radioisotopes. 1997;46(7):450–463. (In Jap.). https://doi.org/10.3769/radioisotopes.46.450.
  70. Zhang S, Pan J, Li Y, Xu C, Zhu C, Wang X, et al. Levels and distributions of radionuclides in soil in China. Chinese Journal of Radiological Medicine and Protection. 1988;8 (2):1–15. (In Chinese).
  71. Pan S, Liu R. Investigation of natural radionuclide contents in soil in China. Radiation Protection. 1992;12(2):122–141.
  72. Stijve T. Potassium content and growth rate of higher fungi. Australasian Mycology Newsletter. 1996;15:70–71.
  73. Potassium [Internet]. [cited 2020 Jun 25]. Available from: https://ods.od.nih.gov/factsheets/Potassium-HealthProfessional.
  74. Commission Implementing Regulation (EU) 2020/1158 of 5 August 2020 on the conditions governing imports of food and feed originating in third countries following the accident at the Chernobyl nuclear power station. Official Journal of the European Union. 2020;13.
  75. Liu D, Cheng H., Bussmann RW, Guo Z, Liu B, Long C. An ethnobotanical survey of edible fungi in Chuxiong City, Yunnan, China. Journal of Ethnobiology and Ethnomedicine. 2018;14(1). https://doi.org/10.1186/s13002-018-0239-2.
How to quote?
Saniewski Michał, Falandysz Jerzy, Zalewska Tamara 137Cs and 40K activity concentrations in edible wild mushrooms from China regions during the 2014–2016 period. Foods and Raw Materials, 2022, vol. 10, no. 1, pp. 86-96
DOI
http://doi.org/10.21603/2308-4057-2022-1-86-96
Publisher
Kemerovo State University
https://kemsu.ru
ISSN
2308-4057 (Print) /
2310-9599 (Online)
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